Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli

Bibliographic Details
Main Author: Soria-Bustos, Jorge
Publication Date: 2021
Other Authors: Saitz, Waleska, Medrano, Abraham, Lara-Ochoa, Cristina, Bennis, Zineb, Monteiro-Neto, Valerio, dos Santos, Camilla Itapary, Rodrigues, Josias [UNESP], Hernandes, Rodrigo T. [UNESP], Yáñez, Jorge A., Torres, Javier, Navarro-García, Fernando, Martínez-Laguna, Ygnacio, Fontes Piazza, Roxane M., Munhoz, Danielle Dias, Cedillo, María L., Ares, Miguel A., De la Cruz, Miguel A., Nataro, James P., Girón, Jorge A.
Format: Article
Language: eng
Source: Repositório Institucional da UNESP
Download full: http://dx.doi.org/10.1111/1462-2920.15737
http://hdl.handle.net/11449/229441
Summary: The interaction of enteroaggregative Escherichia coli (EAEC) strains with the colonic gut mucosa is characterized by the ability of the bacteria to form robust biofilms, to bind mucin, and induce a local inflammatory response. These events are mediated by a repertoire of five different aggregative adherence fimbriae variants (AAF/I-V) typically encoded on virulence plasmids. In this study, we report the production in EAEC strains of a new YehD fimbriae (YDF), which is encoded by the chromosomal gene cluster yehABCD, also present in most E. coli strains. Immuno-labelling of EAEC strain 042 with anti-AAF/II and anti-YDF antibodies demonstrated the presence of both AAF/II and YDF on the bacterial surface. We investigated the role of YDF in cell adherence, biofilm formation, colonization of spinach leaves, and induction of pro-inflammatory cytokines release. To this aim, we constructed yehD deletion mutants in different EAEC backgrounds (strains 17-2, 042, 55989, C1010, 278-1, J7) each harbouring one of the five AAFs. The effect of the YDF mutation was strain dependent and AAF independent as the lack of YDF had a different impact on the phenotypes manifested by the different EAECs tested. Expression of the yehABCD operon in a E. coli K12 ORN172 showed that YDF is important for biofilm formation but not for adherence to HeLa cells. Lastly, screening of pro-inflammatory cytokines in supernatants of Caco-2 cells infected with EAEC strains 042 and J7 and their isogenic ΔyehD mutants showed that these mutants were significantly defective in release of IL-8 and TNF-α. This study contributes to the understanding of the complex and diverse mechanisms of adherence of EAEC strains and identifies a new potential target for preventive measures of gastrointestinal illness caused by EAEC and other E. coli pathogroups.
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spelling Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coliThe interaction of enteroaggregative Escherichia coli (EAEC) strains with the colonic gut mucosa is characterized by the ability of the bacteria to form robust biofilms, to bind mucin, and induce a local inflammatory response. These events are mediated by a repertoire of five different aggregative adherence fimbriae variants (AAF/I-V) typically encoded on virulence plasmids. In this study, we report the production in EAEC strains of a new YehD fimbriae (YDF), which is encoded by the chromosomal gene cluster yehABCD, also present in most E. coli strains. Immuno-labelling of EAEC strain 042 with anti-AAF/II and anti-YDF antibodies demonstrated the presence of both AAF/II and YDF on the bacterial surface. We investigated the role of YDF in cell adherence, biofilm formation, colonization of spinach leaves, and induction of pro-inflammatory cytokines release. To this aim, we constructed yehD deletion mutants in different EAEC backgrounds (strains 17-2, 042, 55989, C1010, 278-1, J7) each harbouring one of the five AAFs. The effect of the YDF mutation was strain dependent and AAF independent as the lack of YDF had a different impact on the phenotypes manifested by the different EAECs tested. Expression of the yehABCD operon in a E. coli K12 ORN172 showed that YDF is important for biofilm formation but not for adherence to HeLa cells. Lastly, screening of pro-inflammatory cytokines in supernatants of Caco-2 cells infected with EAEC strains 042 and J7 and their isogenic ΔyehD mutants showed that these mutants were significantly defective in release of IL-8 and TNF-α. This study contributes to the understanding of the complex and diverse mechanisms of adherence of EAEC strains and identifies a new potential target for preventive measures of gastrointestinal illness caused by EAEC and other E. coli pathogroups.Department of Pediatrics University of Virginia School of MedicineUnidad de Investigación Médica en Enfermedades Infecciosas y Parasitarias Centro Médico Nacional Siglo XXI Instituto Mexicano de Seguro SocialCentro de Detección Biomolecular Benemérita Universidad Autónoma de PueblaUniversity of Florida Emerging Pathogens InstituteDepartamento de Patologia Universidade Federal do MaranhãoDepartamento de Microbiologia e Imunologia Instituto de Biociencias da UNESPFacultad de Estomatología Benemérita Universidad Autónoma de PueblaDepartamento de Biología Celular Centro de Investigaciones Avanzadas Instituto Politécnico NacionalCentro de Investigaciones en Ciencias Microbiológicas Benemérita Universidad Autónoma de PueblaLaboratory of Bacteriology Instituto ButantanDepartamento de Microbiologia e Imunologia Instituto de Biociencias da UNESPUniversity of Virginia School of MedicineInstituto Mexicano de Seguro SocialBenemérita Universidad Autónoma de PueblaEmerging Pathogens InstituteUniversidade Federal do MaranhãoUniversidade Estadual Paulista (UNESP)Instituto Politécnico NacionalInstituto ButantanSoria-Bustos, JorgeSaitz, WaleskaMedrano, AbrahamLara-Ochoa, CristinaBennis, ZinebMonteiro-Neto, Valeriodos Santos, Camilla ItaparyRodrigues, Josias [UNESP]Hernandes, Rodrigo T. [UNESP]Yáñez, Jorge A.Torres, JavierNavarro-García, FernandoMartínez-Laguna, YgnacioFontes Piazza, Roxane M.Munhoz, Danielle DiasCedillo, María L.Ares, Miguel A.De la Cruz, Miguel A.Nataro, James P.Girón, Jorge A.2022-04-29T08:32:35Z2022-04-29T08:32:35Z2021-01-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1111/1462-2920.15737Environmental Microbiology.1462-29201462-2912http://hdl.handle.net/11449/22944110.1111/1462-2920.157372-s2.0-85114024208Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengEnvironmental Microbiologyinfo:eu-repo/semantics/openAccess2022-04-29T08:32:35Zoai:repositorio.unesp.br:11449/229441Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462022-04-29T08:32:35Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli
title Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli
spellingShingle Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli
Soria-Bustos, Jorge
title_short Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli
title_full Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli
title_fullStr Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli
title_full_unstemmed Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli
title_sort Role of the YehD fimbriae in the virulence-associated properties of enteroaggregative Escherichia coli
author Soria-Bustos, Jorge
author_facet Soria-Bustos, Jorge
Saitz, Waleska
Medrano, Abraham
Lara-Ochoa, Cristina
Bennis, Zineb
Monteiro-Neto, Valerio
dos Santos, Camilla Itapary
Rodrigues, Josias [UNESP]
Hernandes, Rodrigo T. [UNESP]
Yáñez, Jorge A.
Torres, Javier
Navarro-García, Fernando
Martínez-Laguna, Ygnacio
Fontes Piazza, Roxane M.
Munhoz, Danielle Dias
Cedillo, María L.
Ares, Miguel A.
De la Cruz, Miguel A.
Nataro, James P.
Girón, Jorge A.
author_role author
author2 Saitz, Waleska
Medrano, Abraham
Lara-Ochoa, Cristina
Bennis, Zineb
Monteiro-Neto, Valerio
dos Santos, Camilla Itapary
Rodrigues, Josias [UNESP]
Hernandes, Rodrigo T. [UNESP]
Yáñez, Jorge A.
Torres, Javier
Navarro-García, Fernando
Martínez-Laguna, Ygnacio
Fontes Piazza, Roxane M.
Munhoz, Danielle Dias
Cedillo, María L.
Ares, Miguel A.
De la Cruz, Miguel A.
Nataro, James P.
Girón, Jorge A.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv University of Virginia School of Medicine
Instituto Mexicano de Seguro Social
Benemérita Universidad Autónoma de Puebla
Emerging Pathogens Institute
Universidade Federal do Maranhão
Universidade Estadual Paulista (UNESP)
Instituto Politécnico Nacional
Instituto Butantan
dc.contributor.author.fl_str_mv Soria-Bustos, Jorge
Saitz, Waleska
Medrano, Abraham
Lara-Ochoa, Cristina
Bennis, Zineb
Monteiro-Neto, Valerio
dos Santos, Camilla Itapary
Rodrigues, Josias [UNESP]
Hernandes, Rodrigo T. [UNESP]
Yáñez, Jorge A.
Torres, Javier
Navarro-García, Fernando
Martínez-Laguna, Ygnacio
Fontes Piazza, Roxane M.
Munhoz, Danielle Dias
Cedillo, María L.
Ares, Miguel A.
De la Cruz, Miguel A.
Nataro, James P.
Girón, Jorge A.
description The interaction of enteroaggregative Escherichia coli (EAEC) strains with the colonic gut mucosa is characterized by the ability of the bacteria to form robust biofilms, to bind mucin, and induce a local inflammatory response. These events are mediated by a repertoire of five different aggregative adherence fimbriae variants (AAF/I-V) typically encoded on virulence plasmids. In this study, we report the production in EAEC strains of a new YehD fimbriae (YDF), which is encoded by the chromosomal gene cluster yehABCD, also present in most E. coli strains. Immuno-labelling of EAEC strain 042 with anti-AAF/II and anti-YDF antibodies demonstrated the presence of both AAF/II and YDF on the bacterial surface. We investigated the role of YDF in cell adherence, biofilm formation, colonization of spinach leaves, and induction of pro-inflammatory cytokines release. To this aim, we constructed yehD deletion mutants in different EAEC backgrounds (strains 17-2, 042, 55989, C1010, 278-1, J7) each harbouring one of the five AAFs. The effect of the YDF mutation was strain dependent and AAF independent as the lack of YDF had a different impact on the phenotypes manifested by the different EAECs tested. Expression of the yehABCD operon in a E. coli K12 ORN172 showed that YDF is important for biofilm formation but not for adherence to HeLa cells. Lastly, screening of pro-inflammatory cytokines in supernatants of Caco-2 cells infected with EAEC strains 042 and J7 and their isogenic ΔyehD mutants showed that these mutants were significantly defective in release of IL-8 and TNF-α. This study contributes to the understanding of the complex and diverse mechanisms of adherence of EAEC strains and identifies a new potential target for preventive measures of gastrointestinal illness caused by EAEC and other E. coli pathogroups.
publishDate 2021
dc.date.none.fl_str_mv 2021-01-01
2022-04-29T08:32:35Z
2022-04-29T08:32:35Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1111/1462-2920.15737
Environmental Microbiology.
1462-2920
1462-2912
http://hdl.handle.net/11449/229441
10.1111/1462-2920.15737
2-s2.0-85114024208
url http://dx.doi.org/10.1111/1462-2920.15737
http://hdl.handle.net/11449/229441
identifier_str_mv Environmental Microbiology.
1462-2920
1462-2912
10.1111/1462-2920.15737
2-s2.0-85114024208
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Environmental Microbiology
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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reponame:Repositório Institucional da UNESP
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reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
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